Ferroptosis in plants: regulation of lipid peroxidation and redox status.

Regulated cell death (RCD) is an essential process that plays key roles along the plant life cycle. Unlike accidental cell death, which is an uncontrolled biological process, RCD involves integrated signaling cascades and precise molecular-mediated mechanisms that are triggered in response to specific exogenous or endogenous stimuli. Ferroptosis is a cell death pathway characterized by the iron-dependent accumulation of lipid reactive oxygen species. Although first described in animals, ferroptosis in plants shares all the main core mechanisms observed for ferroptosis in other systems. In plants as in animals, oxidant and antioxidant systems outline the process of lipid peroxidation during ferroptosis. In plants, cellular compartments such as mitochondria, chloroplasts and cytosol act cooperatively and coordinately to respond to changing redox environments. This particular context makes plants a unique model to study redox status regulation and cell death. In this review, we focus on our most recent understanding of the regulation of redox state and lipid peroxidation in plants and their role during ferroptosis.

A mitochondrial ADXR-ADX-P450 electron transport chain is essential for maternal gametophytic control of embryogenesis in Arabidopsis.

Mitochondrial adrenodoxins (ADXs) are small iron-sulfur proteins with electron transfer properties. In animals, ADXs transfer electrons between an adrenodoxin reductase (ADXR) and mitochondrial P450s, which is crucial for steroidogenesis. Here we show that a plant mitochondrial steroidogenic pathway, dependent on an ADXR-ADX-P450 shuttle, is essential for female gametogenesis and early embryogenesis through a maternal effect. The steroid profile of maternal and gametophytic tissues of wild-type (WT) and adxr ovules revealed that homocastasterone is the main steroid present in WT gametophytes and that its levels are reduced in the mutant ovules. The application of exogenous homocastasterone partially rescued adxr and P450 mutant phenotypes, indicating that gametophytic homocastasterone biosynthesis is affected in the mutants and that a deficiency of this hormone causes the phenotypic alterations observed. These findings also suggest not only a remarkable similarity between steroid biosynthetic pathways in plants and animals but also a common function during sexual reproduction.

Ferroptosis in plants: triggers, proposed mechanisms, and the role of iron in modulating cell death.

Regulated cell death plays key roles during essential processes throughout the plant life cycle. It takes part in specific developmental programs and maintains homeostasis of the organism in response to unfavorable environments. Ferroptosis is a recently discovered iron-dependent cell death pathway characterized by the accumulation of lipid reactive oxygen species. In plants, ferroptosis shares all the main hallmarks described in other systems. Those specific features include biochemical and morphological signatures that seem to be conserved among species. However, plant cells have specific metabolic pathways and a high degree of metabolic compartmentalization. Together with their particular morphology, these features add more complexity to the plant ferroptosis pathway. In this review, we summarize the most recent advances in elucidating the roles of ferroptosis in plants, focusing on specific triggers, the main players, and underlying pathways.

Heat stress in Marchantia polymorpha: Sensing and mechanisms underlying a dynamic response.

Sensing and response to high temperatures are crucial to prevent heat-related damage and to preserve cellular and metabolic functions. The response to heat stress is a complex and coordinated process that involves several subcellular compartments and multi-level regulatory networks that are synchronized to avoid cell damage while maintaining cellular homeostasis. In this review, we provide an insight into the most recent advances in elucidating the molecular mechanisms involved in heat stress sensing and response in Marchantia polymorpha. Based on the signaling pathways and genes that were identified in Marchantia, our analyses indicate that although with specific particularities, the core components of the heat stress response seem conserved in bryophytes and angiosperms. Liverworts not only constitute a powerful tool to study heat stress response and signaling pathways during plant evolution, but also provide key and simple mechanisms to cope with extreme temperatures. Given the increasing prevalence of high temperatures around the world as a result of global warming, this knowledge provides a new set of molecular tools with potential agronomical applications.

A Complex Journey: Cell Wall Remodeling, Interactions, and Integrity During Pollen Tube Growth.

In flowering plants, pollen tubes undergo a journey that starts in the stigma and ends in the ovule with the delivery of the sperm cells to achieve double fertilization. The pollen cell wall plays an essential role to accomplish all the steps required for the successful delivery of the male gametes. This extended path involves female tissue recognition, rapid hydration and germination, polar growth, and a tight regulation of cell wall synthesis and modification, as its properties change not only along the pollen tube but also in response to guidance cues inside the pistil. In this review, we focus on the most recent advances in elucidating the molecular mechanisms involved in the regulation of cell wall synthesis and modification during pollen germination, pollen tube growth, and rupture.

Heat stress induces ferroptosis-like cell death in plants.

In plants, regulated cell death (RCD) plays critical roles during development and is essential for plant-specific responses to abiotic and biotic stresses. Ferroptosis is an iron-dependent, oxidative, nonapoptotic form of cell death recently described in animal cells. In animal cells, this process can be triggered by depletion of glutathione (GSH) and accumulation of lipid reactive oxygen species (ROS). We investigated whether a similar process could be relevant to cell death in plants. Remarkably, heat shock (HS)-induced RCD, but not reproductive or vascular development, was found to involve a ferroptosis-like cell death process. In root cells, HS triggered an iron-dependent cell death pathway that was characterized by depletion of GSH and ascorbic acid and accumulation of cytosolic and lipid ROS. These results suggest a physiological role for this lethal pathway in response to heat stress in Arabidopsis thaliana The similarity of ferroptosis in animal cells and ferroptosis-like death in plants suggests that oxidative, iron-dependent cell death programs may be evolutionarily ancient.

Role of mitochondria during female gametophyte development and fertilization in A. thaliana.

Plants alternate between two generations during their life cycle: the diploid sporophyte and the haploid male and female gametophytes, in which gametes are generated. In higher plants, the female gametophyte or embryo sac is a highly polarized seven-celled structure that develops within the sporophytic tissues of the ovule. It has been proposed that mitochondria are crucial in many cell signaling pathways controlling mitosis, cell specification, cell death and fertilization within the embryo sac. Here, we summarize recent findings that highlight the importance of this organelle during female gametophyte development and fertilization in plants.

New insights into the functional roles of reactive oxygen species during embryo sac development and fertilization in Arabidopsis thaliana.

Previously considered as toxic by-products of aerobic metabolism, reactive oxygen species (ROS) are emerging as essential signaling molecules in eukaryotes. Recent evidence showed that maintenance of ROS homeostasis during female gametophyte development is crucial for embryo sac patterning and fertilization. Although ROS are exclusively detected in the central cell of mature embryo sacs, the study of mutants deficient in ROS homeostasis suggests that controlled oxidative bursts might take place earlier during gametophyte development. Also, a ROS burst that depends on pollination takes place inside the embryo sac. This oxidative response might be required for pollen tube growth arrest and for sperm cell release. In this mini-review, we will focus on new insights into the role of ROS during female gametophyte development and fertilization. Special focus will be made on the mitochondrial Mn-Superoxide dismutase (MSD1), which has been recently reported to be essential for maintaining ROS homeostasis during embryo sac formation.